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Erythropoietin protects the inner blood-retinal barrier by inhibiting microglia phagocytosis via Src/Akt/cofilin signalling in experimental diabetic retinopathy
Journal article   Open access   Peer reviewed

Erythropoietin protects the inner blood-retinal barrier by inhibiting microglia phagocytosis via Src/Akt/cofilin signalling in experimental diabetic retinopathy

Hai Xie, Chaoyang Zhang, Dandan Liu, Qian Yang, Lei Tang, Tianqin Wang, Haibin Tian, Lixia Lu, Jing-Ying Xu, Furong Gao, …
Diabetologia, v 64(1), pp 211-225
Jan 2021
PMID: 33104828
url
https://doi.org/10.1007/s00125-020-05299-xView
Published, Version of Record (VoR)Maybe Open Access (Publisher Bronze) Open

Abstract

Actin Depolymerizing Factors - metabolism Animals Blood-Retinal Barrier - drug effects Blood-Retinal Barrier - physiopathology Cell Hypoxia Coculture Techniques Diabetes Mellitus, Experimental - complications Diabetic Retinopathy - physiopathology Endothelial Cells - metabolism Erythropoietin - administration & dosage Erythropoietin - therapeutic use Humans Intravitreal Injections Male Microglia - physiology Phagocytosis - drug effects Proto-Oncogene Proteins c-akt - metabolism Rats Rats, Sprague-Dawley Signal Transduction - drug effects Signal Transduction - physiology src-Family Kinases - metabolism
Microglial activation in diabetic retinopathy and the protective effect of erythropoietin (EPO) have been extensively studied. However, the regulation of microglia in the retina and its relationship to inner blood-retinal barrier (iBRB) maintenance have not been fully characterised. In this study, we investigated the role of microglia in iBRB breakdown in diabetic retinopathy and the protective effects of EPO in this context. Male Sprague Dawley rats were injected intraperitoneally with streptozotocin (STZ) to establish the experimental model of diabetes. At 2 h after STZ injection, the right and left eyes were injected intravitreally with EPO (16 mU/eye, 2 μl) and an equivalent volume of normal saline (NaCl 154 mmol/l), respectively. The rats were killed at 2 or 8 weeks after diabetes onset. Microglia activation was detected by ionised calcium binding adaptor molecule (IBA)-1 immunolabelling. Leakage of the iBRB was evaluated by albumin staining and FITC-dextran permeability assay. BV cells and primary rat microglia under hypoxic conditions were used to model microglial activation in diabetic retinopathy. Phagocytosis was examined by confocal microscopy in flat-mounted retina preparations and in microglia and endothelial cell cocultures. Protein levels of IBA-1, CD11b, complement component 1r (C1r), and Src/Akt/cofilin signalling pathway components were assessed by western blotting. In diabetic rat retinas, phagocytosis of endothelial cells by activated microglia was observed at 8 weeks, resulting in an increased number of acellular capillaries (increased by 426.5%) and albumin leakage. Under hypoxic conditions, activated microglia transmigrated to the opposite membrane of the transwell, where they disrupted the endothelial cell monolayer by engulfing endothelial cells. The activation and phagocytic activity of microglia was blocked by intravitreal injection of EPO. In vitro, IBA-1, CD11b and C1r protein levels were increased by 50.9%, 170.0% and 135.5%, respectively, by hypoxia, whereas the phosphorylated proteins of Src/Akt/cofilin signalling pathway components were decreased by 74.2%, 47.8% and 39.7%, respectively, compared with the control; EPO treatment abrogated these changes. In experimental diabetic retinopathy, activated microglia penetrate the basement membrane of the iBRB and engulf endothelial cells, leading to iBRB breakdown. EPO exerts a protective effect that preserves iBRB integrity via activation of Src/Akt/cofilin signalling in microglia, as demonstrated in vitro. These data support a causal role for activated microglia in iBRB breakdown and highlight the therapeutic potential of EPO for the treatment of diabetic retinopathy. Graphical abstract.

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Endocrinology & Metabolism
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